An ecophysiological explanation for manganese enrichment in rock varnish

Desert varnish is a dark rock coating that forms in arid environments worldwide. It is highly and selectively enriched in manganese, the mechanism for which has been a long-standing geological mystery. We collected varnish samples from diverse sites across the western United States, examined them in...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 118; no. 25; pp. 1 - 8
Main Authors:	Lingappa, Usha F., Yeager, Chris M., Sharma, Ajay, Lanza, Nina L., Morales, Demosthenes P., Xie, Gary, Atencio, Ashley D., Chadwick, Grayson L., Monteverde, Danielle R., Magyar, John S., Webb, Samuel M., Valentine, Joan Selverstone, Hoffman, Brian M., Fischer, Woodward W.
Format:	Journal Article
Language:	English
Published:	Washington National Academy of Sciences 22-06-2021 Proceedings of the National Academy of Sciences
Series:	From the Cover
Subjects:	Antioxidants Arid environments Aridity Biological Science Biological Sciences Chroococcidiopsis Cyanobacteria desert varnish DNA sequencing Earth Sciences Enrichment Imaging techniques INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY Manganese manganese oxide Metagenomics Microbial activity Microorganisms Oxidative stress Paramagnetic resonance Photosynthesis Physical Sciences Redox properties rock varnish Rocks Speciation
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Summary:	Desert varnish is a dark rock coating that forms in arid environments worldwide. It is highly and selectively enriched in manganese, the mechanism for which has been a long-standing geological mystery. We collected varnish samples from diverse sites across the western United States, examined them in petrographic thin section using microscale chemical imaging techniques, and investigated the associated microbial communities using 16S amplicon and shotgun metagenomic DNA sequencing. Our analyses described a material governed by sunlight, water, and manganese redox cycling that hosts an unusually aerobic microbial ecosystem characterized by a remarkable abundance of photosynthetic Cyanobacteria in the genus Chroococcidiopsis as the major autotrophic constituent. We then showed that diverse Cyanobacteria, including the relevant Chroococcidiopsis taxon, accumulate extraordinary amounts of intracellular manganese—over two orders of magnitude higher manganese content than other cells. The speciation of this manganese determined by advanced paramagnetic resonance techniques suggested that the Cyanobacteria use it as a catalytic antioxidant—a valuable adaptation for coping with the substantial oxidative stress present in this environment. Taken together, these results indicated that the manganese enrichment in varnish is related to its specific uptake and use by likely founding members of varnish microbial communities.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 National Aeronautics and Space Administration (NASA) LA-UR-20-22090 USDOE Laboratory Directed Research and Development (LDRD) Program LDRD 20170414ER; AC02-76SF00515; P41GM103393; 89233218CNA000001 USDOE Office of Science (SC), Basic Energy Sciences (BES) National Institutes of Health (NIH) Reviewers: V.C.C., Johns Hopkins University; and K.H.N., University of Southern California. Contributed by Joan Selverstone Valentine, May 3, 2021 (sent for review December 7, 2020; reviewed by Valeria Cizewski Culotta and Kenneth H. Nealson) Author contributions: U.F.L., C.M.Y., N.L.L., J.S.V., and W.W.F. designed research; U.F.L., C.M.Y., A.S., N.L.L., D.P.M., A.D.A., D.R.M., J.S.M., S.M.W., B.M.H., and W.W.F. performed research; U.F.L., C.M.Y., A.S., G.X., G.L.C., and B.M.H. analyzed data; and U.F.L., J.S.V., and W.W.F. wrote the paper.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.2025188118